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Article

Distribution Characteristics and Influence Factors of Rhizosphere Glomalin-Related Soil Protein in Three Vegetation Types of Helan Mountain, China

by
Hui Hou
1,2,†,
Peixuan Yan
3,†,
Qinmi Xie
1,2,
Hongliang Zhao
3,
Haiying Zhang
1,2,
Yingze Lv
3,
Danbo Pang
1,2,4,
Yang Hu
1,2,4,
Jingyao Li
4,
Fang Wang
5 and
Xilu Ni
1,2,4,*
1
Breeding Base for State Key Laboratory of Land Degradation and Ecological Restoration in Northwest China, School of Ecological and Environment, Ningxia University, Yinchuan 750021, China
2
Key Laboratory of Restoration and Reconstruction of Degraded Ecosystems in Northwestern China of Ministry of Education, Ningxia University, Yinchuan 750021, China
3
College of Agriculture, Ningxia University, Yinchuan 750021, China
4
Ningxia Helan Mountain Forest Ecosystem Orientation Observation Research Station, Yinchuan 750021, China
5
School of Geographical Science and Planning, Ningxia University, Yinchuan 750021, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2022, 13(12), 2092; https://doi.org/10.3390/f13122092
Submission received: 4 November 2022 / Revised: 30 November 2022 / Accepted: 7 December 2022 / Published: 8 December 2022
(This article belongs to the Section Forest Soil)
Browse Figures
Versions Notes

Abstract

:
To reveal distribution characteristics of glomalin-related soil protein (GRSP) and it’s influencing factors under different vegetation types in the drought-tolerant shrubland of Helan Mountain, we chose three vegetation types as study subjects: Stipa breviflora (Grassland, G), Amygdalus mongolica (Shrub, S), and Stipa breviflora-Amygdalus mongolica (Grassland-Shrub, G×S) and bare soil was used as the control (CK). The contents of easily extractable glomalin-related soil protein (EE-GRSP) and total glomalin-related soil protein (T-GRSP), soil physicochemical properties, colonization rate, spore density, and species abundance in the rhizosphere soil were determined. The results indicated that EE-GRSP and T-GRSP showed significant difference (p < 0.05) among vegetation types, with GRSP content highest under G×S (5.68 and 6.27 mg·g−1, respectively) and lowest under CK (3.84 and 4.48 mg·g−1, respectively). EE-GRSP/soil organic carbon (SOC) and T-GRSP/SOC showed no significant difference (p > 0.05). The trends of colonization rate, spore density, and species abundance were the same and were significantly different from those of GRSP content (p < 0.05), with maximum values of 75.6%, 20.7 × 10 g−1, and 29.7, and minimum values of 55.6%, 13.0 × 10 g−1, and 12.7, respectively. Pearson correlation analysis showed that EE-GRSP was significantly positively correlated with SOC, total phosphorus, available phosphorus, and colonization rate (p < 0.05), and it showed an extremely significant positive correlation with available potassium, spore density, and species abundance (p < 0.01). T-GRSP was significantly positively correlated with total phosphorus and available phosphorus (p < 0.05), as well as with soil organic carbon, available potassium, spore density, colonization rate, and species abundance (p < 0.01). The redundancy analysis (RDA) showed similar results. Therefore, the distribution characteristics of GRSP and its influencing factors under different vegetation types in the low elevation area of Helan Mountain were influenced by vegetation types, physicochemical properties of rhizosphere soil, and arbuscular mycorrhizal fungi (AMF) colonization, thus providing a scientific basis for soil quality improvement and vegetation restoration.

1. Introduction

Mycorrhiza is a reciprocal symbiosis between fungi and plant roots, and fungi involved in the formation of mycorrhiza are described as “mycorrhizal”. This system can transfer energy (organic carbon) from plants to fungi and transfer inorganic nutrients from fungi to plants [1]. Arbuscular mycorrhizal fungi (AMF) are mycorrhizal fungi, found in the rhizosphere soil, that can form a mutually beneficial relationship with 80% of vascular plants on land [2]. This symbiosis is an important component of the revegetation process and maintenance of ecosystem function in fragile and degraded ecosystems.
Glomalin-related soil protein (GRSP) is a thermostable glycoprotein produced by AMF [3], and it is widely present in forest, grass, and farmland ecosystems due to the prevalence of AMF. GRSPs are divided into two categories according to the extraction method: total GRSP (T-GRSP) and easily extractable GRSP (EE-GRSP). GRSP is an important component of soil organic carbon and an important source of soil carbon pools [4]; its content is closely related to vegetation type, soil type, and growth of AMF [5]. It has been found that GRSP is a persistent organic substance with a strong cementing effect [6]; it can bond small soil particles into large aggregates and enhance the stability of the soil structure [7]. It plays an important role in the formation of soil aggregates and in maintaining their stability. In addition, GRSP plays a role in the regulation of plant stress resistance, and studies have shown that plant responses to stress are enhanced by increasing levels of GRSP in the soil [8]. GRSP also suppresses the content of soil heavy metals and reduces their toxic effects and potential toxicity to soil organisms and plants in the ecosystem [9].
The Helan Mountain ecosystem is an important natural geographical boundary in China and an important ecological barrier in the arid and semi-arid areas of northwest China. It provides important support for ecosystem security and regional ecosystem services of Helan Mountain. Helan Mountain national nature reserve has typical drought-tolerant shrubs and herbs in the low elevation area of Ningxia Hui Autonomous Region, China, and Amygdalus mongolica (shrub) and Stipa breviflora (grassland) are the main constructive species. These plants are important for windbreak, sand fixation, and landscape, which in turn are important for maintenance and stability of mountain and desert ecosystems. To date, most studies have focused on forests, and farmland ecosystems [10,11,12,13] evaluating only the differences in soil organic carbon and aggregate at different elevations in the Helan Mountains [14]. By contrast, few research have been conducted on GRSP. Therefore, we used typical drought-tolerant vegetation in low-elevation of Helan Mountain to reveal distribution characteristics of GRSP and influencing factors, it can elucidate important role played by GRSP and AMF in rhizosphere soil of typical scrubs, and it can also provide a new theoretical basis for improving soil quality and vegetation restoration in arid and semi-arid areas, China.
Therefore, this study chose rhizosphere soil from three typical vegetation types: A. mongolica, S. breviflora, and S. breviflora-A. mongolica. These were selected from the low-elevation area of Helan Mountain in Ningxia for analysis. Asking the scientific questions: (1) What are characteristics of the differences in GRSP content of rhizosphere soil from three vegetation types? And what is proportion of soil carbon pool? (2) How do soil physiochemical properties and GRSP related properties influence GRSP content of rhizosphere soil? Finally, we reveal the distribution characteristics of GRSP and the influencing factors in the rhizosphere soil of different vegetation types. We provided new ideas for the utilization of AMF resources, improvement of soil quality and structure in the low-elevation mountain ecosystem of Helan Mountain, and vegetation restoration in the arid and semi-arid areas.

2. Materials and Methods

2.1. Study Area

The experimental site was located in the Xiangshuigou small watersheds on the eastern slope of Helan Mountain in Yinchuan City, Ningxia Hui Autonomous Region, China (38°27′–39°30′ N, 105°41′–106°41′ E). This location has a typical continental climate, with mountain climate characteristics. It has an average annual temperature of −0.8 °C, an average annual precipitation of 420 mm, and an average annual evaporation of 2000 mm. Its precipitation is mainly concentrated from June to August, accounting for 60% to 80% of the annual precipitation. The main plant species are shrubs (A. mongolica, Potentilla parvifolia, and Caragana stenophylla) and herbs (S. breviflora, S. tianschanica var. gobica, and Agropyron mongolicum) at the experimental site.

2.2. Experimental Design

Based on the field survey, we selected A. mongolica (S), S. breviflora (G), and S. breviflora-A. mongolica (G×S) as sample plots in May 2021 at an altitude of approximately 1700 m in the Xiangshuigou watershed on the eastern slope of Helan Mountain. No other plants were grown in these plots. Sample plots had five replicates, each with a plot of 5 m × 5 m, while bare soil was chosen as the control (CK). The samples were collected in July 2021. Plants with uniform growth were selected, the rhizosphere soil of S and G was dug by the five-point shaking method, the soil of CK was dug 0–20 cm soil by five-point method, and rhizosphere soil and bare ground soil was mixed well separately, put into sterilized bags, and stored in a refrigerated insulated box. Soil samples were brought back to the laboratory and stored in a refrigerator at −80 °C for the determination of soil AMF community diversity. Some samples were naturally dried and sieved for the determination of soil physicochemical properties and GRSP content. Underground plant roots were washed, dried, and immersed in formaldehyde-acetic acid-ethanol fixative (FAA, 0.5:0.5:9) to determine the mycorrhizal colonization rate.

2.3. Projects and Methods of Determination

2.3.1. Determination of Physicochemical Properties of Soils

We referred to “Soil Agrochemical Analysis” [15]; soil pH was determined by pH meter potential method (water: soil ratio of 5:1); soil organic carbon (SOC) was determined by potassium dichromate oxidation with the external heating method; total nitrogen was determined by semi-micro Kjeldahl method; alkali-hydrolyzable nitrogen (AN) was determined by the alkali-hydrolyzable diffusion method; total phosphorus (TP) was determined by HClO4-H2SO4 digestion and the Mo-Sb colorimetric method; available phosphorus (AP) was determined by NaHCO3 extraction and the Mo-Sb colorimetric method; available potassium (AK) was determined by NH4OAc extraction and the flame photometer method.

2.3.2. Determination of GRSP Content

GRSP extraction and determination were performed according to the method described by Wright and Upadhyaya [3]. First, we weighed a 0.25 g soil sample in a 10 mL plastic centrifuge tube, added 2 mL sodium citrate (20 mmoL·L−1, pH = 7.0) as the extractant of EE-GRSP, shook well, and placed the mixture in an autoclave for 30 min at 121 °C. The supernatant was collected by centrifugation for 6 min at 10,000r·min−1 for measurement. Separately, we weighed a 0.25 g soil sample in a 10 mL plastic centrifuge tube, added 2 mL sodium citrate (50 mmoL·L−1, pH = 7.0) as the extractant of T-GRSP, shook well, and placed in an autoclave for 60 min at 121 °C. The supernatant was collected by centrifugation for 6 min at 10,000 r·min−1 for measurement, reprocessed until no more visible red-brown color appeared, and set aside at 4 °C. Then, 0.5 ml of each of these two types of solutions were added to tubes, and 5 mL filtered Coomassie brilliant blue G-250 stain was added until color development for 10 min. We used a microplate reader (Tecan, Infinite 200Pro, Männedorf, Switzerland) for colorimetry at 595 nm wavelength. Finally, the standard curve was plotted with bovine serum protein solution to calculate the GRSP content.

2.3.3. Determination of AMF Colonization Rate, Spore Density and Species Abundance of Soils

The soil spore density was determined by sucrose centrifugation [16]. First, we weighed 10 g of soil in a 500 mL beaker, added an appropriate amount of distilled water, stirred, and allowed it to stand for 10 s. We then passed it successively through 80 mesh and 400 mesh sieves, rinsed into 50 mL centrifuge tubes with water, and centrifuged at 5000 rpm·min−1 for 10 min. The supernatant was removed, and 50% sucrose solution was added, shaken well, centrifuged at 5000 rpm·min−1 for 10 min, passed through a 400-mesh sieve, and gently washed into labelled petri dishes with distilled water. Finally, the number of soil spores was counted under a light microscope (Olympus BX53, Tokyo, Japan).
Colonization rate was determined using the trypan blue staining method [17]. First, the washed roots of the same thickness were cut into Erlenmeyer flasks in approximately 1 cm pieces, and 10% potassium hydroxide solutions were added to stain the roots in a water bath at 90 °C for 45–60 min, then washed 2–3 times to remove the alkaline solutions. Then, 2% hydrochloric acid was added to acidify the roots at room temperature for 5 min, after which the acid was removed. Then, 0.05% trypan blue solution was added to stain the roots in a water bath at 90 °C for 15 min. The solution was removed and washed 2–3 times, and lactic acid, glycerol, and water solution (1:1:1) were added to decolorize the roots at room temperature for 24 h. Finally, five roots were placed on microscope slides with forceps for examination. This was all repeated three times, and the AMF colonization rate was calculated using an optical microscope (Olympus BX53, Tokyo, Japan). The formula used is as follows:
R C % = ( N I N M ) × 100 %  
In the Formula (1), the RC represents colonization rate, the NI represents number of infested root segments, and the NM represents the total number of roots measured.
Rhizosphere soil samples were sent to Shanghai Majorbio Bio-Pharm Technology Co., Ltd. for AMF species diversity evaluation. The species abundance was defined as the number of AMF species in each soil sample.

2.4. Data Analysis

All statistical analyses were performed using Microsoft Excel (Microsoft, Redmond, Washington, DC, USA). One-way ANOVA with Duncan’s test was performed using SPSS 26 software (IBM SPSS, Chicago, IL, USA) to analyze differences in GRSP content, soil spore density, mycorrhizal colonization rate, species abundance, and soil physicochemical properties among the different vegetation types (p < 0.05). Pearson’s correlation analysis was performed using SPSS 26 software (IBM SPSS, Chicago, IL, USA) and a two-tailed significance test between different variables. Origin 2021 software (Origin Lab, Northampton, MA, USA) was used for plotting, and Canoco5 software (USA) was used for redundancy analysis (RDA). Data are presented as mean ± standard error (SE) (n = 5).

3. Results

3.1. Rhizosphere Soil Physicochemical Properties among Different Vegetation Types

Soil pH was not significantly different among the three vegetation types and CK. SOC content was highest in G×S and lowest in CK, and was significantly different between G, S, and CK (p < 0.05). The soil TN content was highest in G×S and lowest in CK. Soil AN content was highest in G and lowest in CK and was significantly different between S, G×S, and CK (p < 0.05). The soil TP content was highest in G and lowest in CK, and there was a significant difference between S and CK (p < 0.05). Soil AP content was highest in G×S, lowest in CK, and was significantly different between CK and other groups (p < 0.05). Soil AK content was highest in G×S and lowest in S and was significantly different between G, S, and CK (p < 0.05) (Table 1).

3.2. GRSP Distribution Characteristics of Rhizosphere Soil among Different Vegetation Types

The EE-GRSP and T-GRSP contents differed among the three vegetation types. EE-GRSP and T-GRSP contents were highest in G×S (5.68 and 6.27 mg·g−1, respectively), followed by G and S; the smallest was in CK (3.84 and 4.48 mg·g−1, respectively). Significant differences were found between G×S and other vegetation types (p < 0.05), whereas the ratios of EE-GRSP and T-GRSP were not significantly different between all types (p > 0.05), with a mean value of 90.33% (Figure 1).
Proportions of EE-GRSP and T-GRSP to SOC were not significantly different (p > 0.05) among the three vegetation types, and their mean values were 41% and 46%, respectively (Table 2).

3.3. Differences of AMF Colonization Rate, Spore Density and Species Abundance among Different Vegetation Types

AMF colonization rate was highest under G×S in the rhizosphere soil of the three vegetation types, followed by G, and smallest under S. Significant differences were found among all types (p < 0.05). Soil spore density and species abundance showed the same trend, being at a maximum under G×S and a minimum under CK and were significantly different (p < 0.05) (Table 3, Figure 2).

3.4. Correlation Analysis of GRSP and Soil Factors

The results of the correlation analysis showed that EE-GRSP had significant positive correlation with SOC, TP, AP and EE-GRSP/SOC, and extremely significant positive correlation with AK, spore density, colonization rate, and species abundance. T-GRSP was in significant positive correlation with TP, AP, and colonization rate, and showed extremely significant positive correlation with SOC, AK, EE-GRSP, spore density, and species abundance. EE-GRSP/SOC was in significant positive correlation with EE-GRSP, while T-GRSP/SOC was extremely significant positive correlation with EE-GRSP/SOC (Figure 3).

3.5. Redundancy Analysis of GRSP and Soil Factors

EE-GRSP, T-GRSP, EE-GRSP/SOC, and T-GRSP/SOC were used as response variables, and soil physicochemical properties, colonization rate, spore density, and species abundance were used as explanatory variables to perform RDA on two sets of data. The results showed that Axis 1 explained 95.23% of the differences in GRSP characteristics, Axis 2 explained 2.91% of the differences in GRSP characteristics, for a cumulative explanation of 98.14%. EE-GRSP and T-GRSP were positively correlated with SOC, TN, pH, AK, TP, AP, species abundance, spore density, and colonization rate; EE-GRSP/SOC and T-GRSP/SOC were positively correlated with AN, AP, TP, colonization rate, species abundance, and spore density; and EE-GRSP/SOC was not correlated with SOC. Spore density (77.1% explained, p = 0.002) and AK (9.7% explained, p = 0.018) had a significant effect on EE-GRSP, T-GRSP, EE-GRSP/SOC, and T-GRSP/SOC. (Figure 4).

4. Discussion

4.1. Distribution of Rhizosphere Soil Nutrients and Their Colonization Rate, Spore Density and Species Abundance among Different Vegetation Types

Because S. breviflora-A. mongolica communities have appreciable plant roots and apoplastic material input [18,19], we found that the G×S community had a higher rhizosphere soil nutrient content than bare ground or the other two mono-vegetation samples, except for soil AN and TP, which was the same as the results for arid valleys [20]. In this study, the colonization rate, spore density, and species abundance of rhizosphere soil AMF in S. breviflora-A. mongolica communities were significantly higher than those of other sample site types, indicating that the soil AMF communities were promoted by the creation of a more favorable soil environment by S. breviflora-A. mongolica communities; these findings are similar to results obtained for the Patagonian steppe [21]. Although AMF characteristics were present in the bare ground, the lowest species abundance and spore density characteristics there suggest that the bare ground was relatively unsuitable for AMF survival.

4.2. Distribution of GRSP in Rhizosphere Soil among Different Vegetation Types

The content and composition of GRSP are influenced by various factors, such as AMF composition, soil type, and vegetation type [22]. The study results showed that AMF colonization and GRSP distribution could be detected under shrubs (S), grasses (G), and grasses with shrubs (G×S) at the low elevation of Helan Mountain, indicating that all vegetation types could form good symbiosis with AMF and secrete GRSP. The mean content of EE-GRSP and T-GRSP were 4.69 mg·g−1 and 5.19 mg·g−1 in the study, respectively, similar to the findings of He et al. [23] and Gałązka et al. [24], compared to the higher GRSP content in ecosystems such as the desert in north China and loess plateau in western Shanxi province [25,26]. This indicates that, likely due to the rich diversity of vegetation, stable environment, and limited human interference at the low elevation of Helan Mountain, its rich plant resources can provide good external conditions for the growth of AMF, which is conducive to the release of GRSP from AMF into the soil [27]. The study showed that EE-GRSP and T-GRSP differed in the rhizosphere soil of different vegetation types, and that their contents were highest among shrubs and lowest on bare ground. This was similar to the findings of Di et al. [28] in the Hujia Mountains of Danjiangkou City, and Gomes et al. [29], because the roots were more intensive in the soil under cover of shrub-grass vegetation, which is conducive to AMF colonization of plant roots and the formation of symbiosis, thus increasing the release of GRSP. However, the trends in GRSP content obtained were grasses > shrubs, which was different from the results of Di et al. [28], who found that the magnitude of GRSP content was shrubs > grasses. The analysis concluded that plant diversity was high, the vegetation cover was more uniform in the sample sites of grasses and shrubs, and the roots of shrubs were more developed than those of herbs. In contrast, there was only one plant in the grass and shrub sample plots in this experiment, but the roots of S. breviflora had more roots than those of A. mongolica, so there was a situation in which the GRSP content of grasses was greater than that of shrubs. The experimental area of the soil type was mountain greyzemic phaeozem, and Glomus was the dominant genus in the previous study under the rhizosphere soil of three vegetation types, indicating that the distribution difference of GRSP content was mainly influenced by different vegetation types and soil factors.
EE-GRSP is the newly produced or soon decomposed fraction of GRSP in soil, while T-GRSP is the sum of newly produced and always preserved GRSP in soil [30]. The turnover time of GRSP in soil can range from 6 to 42 years [31]. In this study, the EE-GRSP/T-GRSP was not significantly different among vegetation types, indicating that there was no significant variation in the ability of AMF to secrete GRSP in rhizosphere soil of three vegetation types at low elevation in Helan Mountain, which was the same as the results of the southern subtropical forest [32]. However, results of our study showed that EE-GRSP/T-GRSP had a mean value of 90.33%, which was higher than that of related studies with 39%–60% [33], which could reflect a higher capacity of AMF to release GRSP recently.
Different vegetation types affect SOC storage [34], and GRSP is an important component of soil organic carbon. The results of the study showed that SOC content and GRSP content had the same trend, and SOC content was low compared to SOC content in forest ecosystems [35], whereas GRSP content was high, resulting in high EE-GRSP/SOC and T-GRSP/SOC, 37.37%–45.03%, and 43.53%–47.88%. There was no significant difference in the proportion of GRSP to SOC among vegetation types, which is inconsistent with the results of Xiao et al. [36] in the Loess Plateau, probably because of conditions such as low plant litter and poor soil development in the study area. SOC content was the only significant difference between shrubs and other vegetation types, and the contribution of GRSP to SOC was found to be more than 20 times higher than that of microbial biomass according to the study [37], so contribution of GRSP to SOC was greater, leading to a higher proportion of GRSP to SOC in the results of this study.

4.3. Influencing Factors of GRSP in Rhizosphere Soil among Different Vegetation Types

The results of the Pearson correlation analysis and RDA showed that EE-GRSP and T-GRSP were significantly and positively correlated with SOC, TP, AP, AK, spore density, colonization rate, and species abundance, and that EE-GRSP/SOC and T-GRSP/SOC were negatively correlated with SOC and pH and positively correlated with other soil physicochemical properties and AMF colonization rate, which is generally consistent with Singh et al. [38] in arid areas. EE-GRSP and T-GRSP showed significant and extremely significant positive correlations with SOC, respectively, indicating a strong correlation between GRSP and SOC. Related studies have shown that soil pH can affect mycorrhizal formation and GRSP secretion; AMF growth and development are preferred in slightly acidic soils [39], and pH is negatively correlated with GRSP or spore density. However, the results of this study showed that soil pH was 8.21~8.30, and there was no significant relationship between GRSP and pH, probably because pH variation was small, and Glomus had a dominant position, which occurred in the pH range of 5 to 9 [40], consistent with the environment required for growth and development of Glomus. It was found that soil TN increased significantly after AMF inoculation, and secreted GRSP contributed to increased soil TN [41], and GRSP content first increased and then decreased with increase of phosphorus level [42], was consistent with the results of study that GRSP was positively correlated with soil TN and AN and significant positive correlation with TP and AP.GRSP was mainly found in the AMF mycelium and spore wall layer [43]; when plant roots had a high colonization rate, soil also had a high GRSP content generally. Colonization rate, spore density, and species abundance were significantly or extremely significantly positively correlated with GRSP, with the same trend as GRSP, with mean values of 65.19%, 17.08a × 10 g−1, and 22.50, indicating that the effects of colonization rate and others on GRSP were crucial. Differences in vegetation types affected the composition and colonization of AMF, thus influencing the GRSP content, which was the same as the findings of Zhang et al. [44] in tropical montane rainforests. This study can further reveal the factors influencing GRSP distribution characteristics by adding indicators such as soil water content, climatic factors, and GRSP content of the soil layer at different depths.

5. Conclusions

GRSP was detected in the rhizosphere soil of three vegetation types in the low-elevation area of the Helan Mountain National Nature Reserve in Ningxia, and different vegetation types significantly affected the distribution of GRSP content. The trends of both EE-GRSP and T-GRSP contents were G×S > G > S > CK, with mean contents of 4.69 mg·g−1 and 5.19 mg·g−1, respectively, whereas EE-GRSP/T-GRSP, EE-GRSP/SOC and T-GRSP/SOC did not differ significantly among vegetation types, indicating that the rhizosphere soil AMF releasing GRSP was basically the same among vegetation types and GRSP was an important component of the soil carbon pool in the low-elevation area of Helan Mountain. GRSP content is closely related to soil physicochemical properties, spore density, AMF colonization rate and species abundance. This study reveals the distribution characteristics of GRSP and influencing factors under three vegetation types in the low-altitude area of the Helan Mountain National Nature Reserve in Ningxia, which is important for improving soil quality as well as vegetation restoration in the area.

Author Contributions

Data curation, H.H.; Funding acquisition, X.N.; Investigation, H.H., P.Y., Q.X., H.Z. (Hongliang Zhao), H.Z. (Haiying Zhang), Y.L., D.P., Y.H., J.L., F.W. and X.N.; Resources, X.N.; Software, H.H.; Supervision, X.N.; Validation, X.N.; Visualization, H.H.; Writing—original draft, H.H. and P.Y.; Writing—review and editing, H.H., P.Y., X.N. All coauthors contributed to the discussion, revision, and improvement of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Key Project of Research and Development of Ningxia, China (2020BFG03006, 2021BEG02005), the National Natural Science Foundation of Ningxia, China (2020AAC03107, 2020AAC03085), and the National Natural Science Foundation of China (41761066, 42067022).

Data Availability Statement

Not applicable.

Acknowledgments

We thank the Helan Mountain National Nature Reserve Administration in Ningxia and the staff of the Suyukou Management Station for their assistance.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 13 02092 g001 550
Figure 1. Distribution characteristics of EE-GRSP and T-GRSP of rhizosphere soil among different vegetation types. Different lowercase letters indicate significant differences between plots (p < 0.05).
Figure 1. Distribution characteristics of EE-GRSP and T-GRSP of rhizosphere soil among different vegetation types. Different lowercase letters indicate significant differences between plots (p < 0.05).
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Forests 13 02092 g002 550
Figure 2. (a) Magnification of AMF soil spores and (b) colonization infection. In panel (a), A designates spores (4×, 200 μm); In panel (b), A designates vesicles; B, hyphae; and C, arbuscules (20×, 50 μm).
Figure 2. (a) Magnification of AMF soil spores and (b) colonization infection. In panel (a), A designates spores (4×, 200 μm); In panel (b), A designates vesicles; B, hyphae; and C, arbuscules (20×, 50 μm).
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Forests 13 02092 g003 550
Figure 3. Pearson correlation analysis between GRSP and environmental factors. EEG, EE-GRSP; TG, T-GRSP; E/S, EE-GRSP/SOC; T/S, T-GRSP/SOC; SD, spore density; CR, colonization rate; SA, species abundance. The same below. *, p < 0.05; **, p < 0.01.
Figure 3. Pearson correlation analysis between GRSP and environmental factors. EEG, EE-GRSP; TG, T-GRSP; E/S, EE-GRSP/SOC; T/S, T-GRSP/SOC; SD, spore density; CR, colonization rate; SA, species abundance. The same below. *, p < 0.05; **, p < 0.01.
Forests 13 02092 g003
Forests 13 02092 g004 550
Figure 4. Redundancy analysis of GRSP and environmental factors. Hollow arrows point to explanatory variables; solid arrows point to response variables.
Figure 4. Redundancy analysis of GRSP and environmental factors. Hollow arrows point to explanatory variables; solid arrows point to response variables.
Forests 13 02092 g004
Table
Table 1. Physicochemical properties of rhizosphere soil of different vegetation types.
Table 1. Physicochemical properties of rhizosphere soil of different vegetation types.
PlotspHSOC
(g·kg−1)		TN
(mg·kg−1)		AN
(mg·kg−1)		TP
(mg·kg−1)		AP
(mg·kg−1)		AK
(mg·kg−1)
G8.2 ± 0.0 a11.1 ± 0.5 b30.8 ± 9.0 a56.9 ± 1.8 a242.5 ± 8.4 a7.4 ± 1.7 ab168.2 ± 5.3 b
S8.2 ± 0.0 a10.7 ± 0.7 b29.9 ± 3.4 a27.7 ± 2.6 c123.9 ± 1.5 b6.0 ± 0.5 ab94.8 ± 14.4 c
G×S8.3 ± 0.0 a13.4 ± 0.1 a41.1 ± 9.7 a37.8 ± 0.6 b184.9 ± 4.0 ab9.0 ± 0.2 a244.3 ± 7.1 a
CK8.2 ± 0.1 a10.3 ± 0.2 b27.1 ± 3.4 a24.4 ± 2.2 c49.2 ± 17.7 c4.2 ± 0.7 b116.2 ± 2.7 c
G represents grass, S represents shrubs, G×S represents grasses-shrubs, and CK represents bare soil without plants. Different lowercase letters indicate significant differences between treatments in the same column (p < 0.05). Values are mean ± standard error (SE) (n = 5). The same below.
Table
Table 2. Ratio of GRSP to SOC of rhizosphere soil among different vegetation types.
Table 2. Ratio of GRSP to SOC of rhizosphere soil among different vegetation types.
PlotsEE-GRSP/SOC
(%)		T-GRSP/SOC
(%)
G45 ± 5 a48 ± 3 a
S41 ± 3 a44 ± 3 a
G×S42 ± 1 a47 ± 0 a
CK37 ± 1 a44 ± 0 a
Different lowercase letters indicate significant differences between treatments in the same column (p < 0.05).
Table
Table 3. Differences of AMF colonization rate, spore density, and species abundance among different vegetation types.
Table 3. Differences of AMF colonization rate, spore density, and species abundance among different vegetation types.
PlotsColonization Rate
(%)		Spore Density
(10 g−1)		Species Abundance
G64.4 ± 5.9 ab18.3 ± 0.3 b26.0 ± 1.0 ab
S55.6 ± 4.4 b16.3 ± 0.3 c21.7 ± 1.2 b
G×S75.6 ± 2.2 a20.7 ± 0.9 a29.7 ± 0.9 a
CK-13.0 ± 0.6 d12.7 ± 2.9 c
Different lowercase letters indicate significant differences between treatments in the same column (p < 0.05). “-” indicates that there is no data.
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Hou, H.; Yan, P.; Xie, Q.; Zhao, H.; Zhang, H.; Lv, Y.; Pang, D.; Hu, Y.; Li, J.; Wang, F.; et al. Distribution Characteristics and Influence Factors of Rhizosphere Glomalin-Related Soil Protein in Three Vegetation Types of Helan Mountain, China. Forests 2022, 13, 2092. https://doi.org/10.3390/f13122092

AMA Style

Hou H, Yan P, Xie Q, Zhao H, Zhang H, Lv Y, Pang D, Hu Y, Li J, Wang F, et al. Distribution Characteristics and Influence Factors of Rhizosphere Glomalin-Related Soil Protein in Three Vegetation Types of Helan Mountain, China. Forests. 2022; 13(12):2092. https://doi.org/10.3390/f13122092

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Hou, Hui, Peixuan Yan, Qinmi Xie, Hongliang Zhao, Haiying Zhang, Yingze Lv, Danbo Pang, Yang Hu, Jingyao Li, Fang Wang, and et al. 2022. "Distribution Characteristics and Influence Factors of Rhizosphere Glomalin-Related Soil Protein in Three Vegetation Types of Helan Mountain, China" Forests 13, no. 12: 2092. https://doi.org/10.3390/f13122092

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